Enrichment of GABARAP Relative to LC3 in the Axonal Initial Segments of Neurons

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Koike, Masato ^a   Tanida, Isei ^a,b   Nanao, Tomohisa ^a   Tada, Norihiro ^a   Iwata, Jun Ichi ^a   Ueno, Takashi ^a   Kominami, Eiki ^a   Uchiyama, Yasuo ^a  

^a JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ASSOCIATED PROTEIN; BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; DENDRITE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; NERVE CELL; NONHUMAN; PERIKARYON; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PURKINJE CELL; PYRAMIDAL NERVE CELL;

ANIMALS; AXONS; CEREBELLUM; CYTOSKELETAL PROTEINS; DENDRITES; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSOMES; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; PURKINJE CELLS; PYRAMIDAL CELLS; SYNAPTIC VESICLES;

EID: 84877354086     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063568     Document Type: Article

References (46)

1. Wang H, Bedford FK, Brandon NJ, Moss SJ, Olsen RW, (1999) GABAA-receptor-associated protein links GABAA receptors and the cytoskeleton. Nature 397: 69-72.
2. Chen ZW, Olsen RW, (2007) GABAA receptor associated proteins: a key factor regulating GABAA receptor function. J Neurochem 100: 279-294.
3. Kneussel M, Haverkamp S, Fuhrmann JC, Wang H, Wassle H, et al. (2000) The gamma-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc Natl Acad Sci U S A 97: 8594-8599.
4. Okazaki N, Yan J, Yuasa S, Ueno T, Kominami E, et al. (2000) Interaction of the Unc-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: possible role of vesicular transport in axonal elongation. Brain Res Mol Brain Res 85: 1-12.
5. Green F, O'Hare T, Blackwell A, Enns CA, (2002) Association of human transferrin receptor with GABARAP. FEBS Lett 518: 101-106.
6. Kanematsu T, Jang IS, Yamaguchi T, Nagahama H, Yoshimura K, et al. (2002) Role of the PLC-related, catalytically inactive protein p130 in GABAA receptor function. EMBO J 21: 1004-1011.
7. Kouno T, Mizuguchi M, Tanida I, Ueno T, Kanematsu T, et al. (2005) Solution structure of microtubule-associated protein light chain 3 and identification of its functional subdomains. J Biol Chem 280: 24610-24617.
8. Schwarten M, Mohrluder J, Ma P, Stoldt M, Thielmann Y, et al. (2009) Nix directly binds to GABARAP: A possible crosstalk between apoptosis and autophagy. Autophagy 5: 690-698.
9. Reining SC, Gisler SM, Fuster D, Moe OW, O'Sullivan GA, et al. (2009) GABARAP deficiency modulates expression of NaPi-IIa in renal brush-border membranes. Am J Physiol Renal Physiol 296: F1118-1128.
10. Tanida I, Komatsu M, Ueno T, Kominami E, (2003) GATE-16 and GABARAP are authentic modifiers mediated by Apg7 and Apg3. Biochem Biophys Res Commun 300: 637-644.
11. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, et al. (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 117: 2805-2812.
12. Legesse-Miller A, Sagiv Y, Porat A, Elazar Z, (1998) Isolation and characterization of a novel low molecular weight protein involved in intra-Golgi traffic. J Biol Chem 273: 3105-3109.
13. Sagiv Y, Legesse-Miller A, Porat A, Elazar Z, (2000) GATE-16, a membrane transport modulator, interacts with NSF and the Golgi v-SNARE GOS-28. EMBO J 19: 1494-1504.
14. Vernier-Magnin S, Muller S, Sallot M, Radom J, Musard JF, et al. (2001) A novel early estrogen-regulated gene gec1 encodes a protein related to GABARAP. Biochem Biophys Res Commun 284: 118-125.
15. Tanida I, Ueno T, Kominami E, (2004) LC3 conjugation system in mammalian autophagy. Int J Biochem Cell Biol 36: 2503-2518.
16. Tanida I, Sou YS, Minematsu-Ikeguchi N, Ueno T, Kominami E, (2006) Atg8L/Apg8L is the fourth mammalian modifier of mammalian Atg8 conjugation mediated by human Atg4B, Atg7 and Atg3. FEBS J 273: 2553-2562.
17. Tanida I, Tanida-Miyake E, Ueno T, Kominami E, (2001) The human homolog of Saccharomyces cerevisiae Apg7p is a Protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J Biol Chem 276: 1701-1706.
18. Tanida I, Tanida-Miyake E, Komatsu M, Ueno T, Kominami E, (2002) Human Apg3p/Aut1p homologue is an authentic E2 enzyme for multiple substrates, GATE-16, GABARAP, and MAP-LC3, and facilitates the conjugation of hApg12p to hApg5p. J Biol Chem 277: 13739-13744.
19. Tanida I, Sou YS, Ezaki J, Minematsu-Ikeguchi N, Ueno T, et al. (2004) HsAtg4B/HsApg4B/autophagin-1 cleaves the carboxyl termini of three human Atg8 homologues and delipidates microtubule-associated protein light chain 3- and GABAA receptor-associated protein-phospholipid conjugates. J Biol Chem 279: 36268-36276.
20. Sou YS, Tanida I, Komatsu M, Ueno T, Kominami E, (2006) Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP, and GATE-16. J Biol Chem 281: 3017-3024.
21. Tanida I, Wakabayashi M, Kanematsu T, Minematsu-Ikeguchi N, Sou YS, et al. (2006) Lysosomal turnover of GABARAP-phospholipid conjugate is activated during differentiation of C2C12 cells to myotubes without inactivation of the mTor kinase-signaling pathway. Autophagy 2: 264-271.
22. Takagi-Akiba M, Asanuma K, Tanida I, Tada N, Oliva Trejo JA, et al. (2012) Doxorubicin-induced glomerulosclerosis with proteinuria in GFP-GABARAP transgenic mice. Am J Physiol Renal Physiol 302: F380-389.
23. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y, (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15: 1101-1111.
24. Marino G, Salvador-Montoliu N, Fueyo A, Knecht E, Mizushima N, et al. (2007) Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in ATG4C/autophagin-3. J Biol Chem 282: 18573-18583.
25. Kittler JT, Rostaing P, Schiavo G, Fritschy JM, Olsen R, et al. (2001) The subcellular distribution of GABARAP and its ability to interact with NSF suggest a role for this protein in the intracellular transport of GABAA receptors. Mol Cell Neurosci 18: 13-25.
26. Kordeli E, Lambert S, Bennett V, (1995) AnkyrinG. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J Biol Chem 270: 2352-2359.
27. Clark BD, Goldberg EM, Rudy B, (2009) Electrogenic tuning of the axon initial segment. Neuroscientist 15: 651-668.
28. Koike M, Shibata M, Waguri S, Yoshimura K, Tanida I, et al. (2005) Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (batten disease). Am J Pathol 167: 1713-1728.
29. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, et al. (2008) Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172: 454-469.
30. Yue Z, Holstein GR, Chait BT, Wang QJ, (2009) Using genetic mouse models to study the biology and pathology of autophagy in the central nervous system. Methods Enzymol 453: 159-180.
31. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, et al. (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131: 1149-1163.
32. Buffington SA, Rasband MN, (2011) The axon initial segment in nervous system disease and injury. Eur J Neurosci 34: 1609-1619.
33. Nusser Z, (2009) Variability in the subcellular distribution of ion channels increases neuronal diversity. Trends Neurosci 32: 267-274.
34. DeFelipe J, Hendry SH, Jones EG, Schmechel D, (1985) Variability in the terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex. J Comp Neurol 231: 364-384.
35. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P, (1996) Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci U S A 93: 11939-11944.
36. Iwakura A, Uchigashima M, Miyazaki T, Yamasaki M, Watanabe M, (2012) Lack of molecular-anatomical evidence for GABAergic influence on axon initial segment of cerebellar Purkinje cells by the pinceau formation. J Neurosci 32: 9438-9448.
37. Chen L, Wang H, Vicini S, Olsen RW, (2000) The gamma-aminobutyric acid type A (GABAA) receptor-associated protein (GABARAP) promotes GABAA receptor clustering and modulates the channel kinetics. Proc Natl Acad Sci U S A 97: 11557-11562.
38. O'Sullivan GA, Kneussel M, Elazar Z, Betz H, (2005) GABARAP is not essential for GABA receptor targeting to the synapse. Eur J Neurosci 22: 2644-2648.
39. Cook JL, Re RN, deHaro DL, Abadie JM, Peters M, et al. (2008) The trafficking protein GABARAP binds to and enhances plasma membrane expression and function of the angiotensin II type 1 receptor. Circ Res 102: 1539-1547.
40. Lainez S, Valente P, Ontoria-Oviedo I, Estevez-Herrera J, Camprubi-Robles M, et al. (2010) GABAA receptor associated protein (GABARAP) modulates TRPV1 expression and channel function and desensitization. FASEB J 24: 1958-1970.
41. Chen C, Wang Y, Huang P, Liu-Chen LY, (2011) Effects of C-terminal modifications of GEC1 protein and gamma-aminobutyric acid type A (GABAA) receptor-associated protein (GABARAP), two microtubule-associated proteins, on kappa opioid receptor expression. J Biol Chem 286: 15106-15115.
42. Nakajima K, Yin X, Takei Y, Seog DH, Homma N, et al. (2012) Molecular motor KIF5A is essential for GABAA receptor transport, and KIF5A. Neuron 76: 945-961.
43. Nakata T, Hirokawa N, (2003) Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J Cell Biol 162: 1045-1055.
44. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E, (2005) Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1: 84-91.
45. Hell JW, Jahn R (2005) Preparation of synaptic vesicles from mammalian brain. In: Celis JE, Carter N, Simons K, Small JV, Hunter T et al., editors. Cell Biology, Four-Volume Set: A Laboratory Handbook: ELSEVIER. pp. 85-90.
46. Niwa H, Yamamura K, Miyazaki J, (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199.